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Original Article Diallyl Trisulfide Inhibits Proliferation and Promotes Apoptosis of Side Population Cells in Multiple Myeloma Cells

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Original Article Diallyl Trisulfide Inhibits Proliferation and Promotes Apoptosis of Side Population Cells in Multiple Myeloma Cells Int J Clin Exp Med 2017;10(3):5749-5756 www.ijcem.com /ISSN:1940-5901/IJCEM0038165 Original Article Diallyl trisulfide inhibits proliferation and promotes apoptosis of side population cells in multiple myeloma cells Junquan Zeng1, Tingting Liu2, Yongliang Zheng1, Bin Liu1, Mushui Fang1, Shengping Long1, Yijian Chen3 1Department of Hematology, The Affiliated Hospital of Jinggangshan University, Ji’an 343000, Jiangxi Province, China; 2Department of Hematology, Jiangxi Provincial People’s Hospital, Nanchang 330006, Jiangxi Province, China; 3Department of Hematology, The First Affiliated Hospital of Gannan Medical University, Ganzhou 341000, Jiangxi Province, China Received August 18, 2016; Accepted October 24, 2016; Epub March 15, 2017; Published March 30, 2017 Abstract: Multiple myeloma (MM) is an incurable cancer, in which the main factors leading to death are relapse and the development of resistance to drugs. Both of these are associated with the existence of side population (SP) cells, which have features similar to those of tumor stem cells. The development of new safe agents, possibly from natural products, is necessary to more efficiently treat SP cells involved in MM. Diallyl trisulfide (DATS), a natural organosulfur compound isolated from garlic, has been shown to inhibit the occurrence and development of tumors and cancer stem cells and enhance chemosensitivity. However, the effect of DATS on MM proliferation and the biological behavior of SP cells remain unclear. Therefore, in this study, human MM RPMI-8226 and NCI-H929 cell lines were treated with different concentrations of DATS (2, 5, 10, 20, 40, or 80 μM) for 1, 2, or 3 days and the half-maximal inhibitory concentration (IC50) was evaluated using a 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltet- razolium bromide (MTT) assay. In addition, SP RPMI-8226 and NCI-H929 cells were isolated and analyzed using flow cytometry. The effects of dimethyl sulfoxide (DMSO), DATS, and bortezomib on the percentage of MM SP cells, survival rate, colony formation, cell cycle, and cell apoptosis were analyzed using an MTT assay, a colony assay, and flow cytometry analysis. DATS displayed a dose- and time-dependent effect on the survival rate of RPMI-8226 and NCI-H929 cells. DATS and bortezomib treatment reduced the percentage of MM SP cells and the SP cell survival rate and inhibited colony formation and the cell cycle. In addition, DATS and bortezomib treatment promoted SP cell apoptosis. In conclusion, DATS inhibited the proliferation and promoted the apoptosis of SP MM cells. Keywords: Multiple myeloma, diallyl trisulfide, bortezomib, side population cells Introduction and drug resistance are associated with the existence of tumor stem cells. Side population Multiple myeloma (MM), a type of cancer that (SP) cells have features similar to those of affects the plasma cells in the bone marrow, cancer stem cells and have been identified in is the second most common hematological MM using flow cytometry along with Hoechst- cancer worldwide [1]. The number of new MM 33342 staining [4-6]. In MM, SP cells have cases is 6.3 per 100000 persons per year and important pathophysiological and clinical impli- the mortality rate is 3.3 deaths per 100000 cations. Therefore, inhibiting the proliferation persons per year [2]. Currently, MM is treated and promoting the apoptosis of SP cells could with chemotherapy and radiation, which have reduce drug resistance and cancer recurrence, improved the survival rate of patients with thereby prolonging the tumor-free interval in MM. However, the disease remains incurable patients and improving survival rates [7-10]. and has a 5-year survival rate of approxima- Bortezomib, a proteasome inhibitor, reduced tely 47% [3]. Tumor relapse and drug resistan- SP cell numbers by suppressing proliferation ce are the main factors leading to death in through inhibition of the cell cycle. However, patients with MM. In addition, tumor relapse the drug has obvious toxic and side effects DATS inhibits proliferation of side population cells in MM cells [11]. Therefore, the development of new safer Chromadex, Irvine, CA, USA) and incubated in a agents, possibly from natural products, is nec- 96-well plate in a final volume of 0.1 ml at 37°C essary for the efficient treatment of SP cells in for 0, 24, 48, and 72 h. Thereafter, 10 μl of MTT MM. reagent was added to each well and the plate was incubated for 4 h at 37°C. The absorbance Diallyl trisulfide (DATS), a natural organosulfur was measured using a Vmax microplate spec- compound isolated from garlic, has been widely trophotometer (Molecular Devices, Sunnyvale, used in China for more than a thousand years CA, USA) at 570 nm. Each sample was assayed [12]. Recorded history attests that garlic was in triplicate. used to stimulate the immune system, prevent or treat various diseases, and promote health Groups and treatment [13, 14]. In numerous cancer types, DATS inhib- ited the occurrence and development of tumors SP cells were treated with four drugs: DATS, by inhibiting cell proliferation, migration, and bortezomib (10 nm/L, Selleck Chemicals LLC, invasion, arresting the cell cycle, and promoting Houston, TX, USA) as a positive control, and apoptosis [15, 16]. DATS also inhibited cancer 0.1% dimethyl sulfoxide (DMSO) as a negative stem cells and enhanced chemosensitivity [17, control. Cells were harvested after treatment 18]. However, the effect of DATS on MM prolif- following each assay. eration and the biological behavior of SP cells are still unclear. Hoechst33342 fluorescent staining Therefore, in this study, MM cells were treated SP cells were sorted from the MM RPMI-8226 with DATS to determine its effect on the surviv- and NCI-H929 cell lines using the Hoechst- al rate of MM cells. In addition, SP cells were 33342 fluorescent staining method with flow sorted from MM cells and treated with DATS to cytometry. The RPMI-8226 and NCI-H929 cells determine the effect of DATS on the biological were seeded into six-well plates, cultured for behavior of SP cells. The results indicated that 48 h, and 10 μg/ml Hoechst33342 stain (Sig- DATS inhibited the survival of MM cells and ma-Aldrich, St. Louis, MO, USA) was added. The decreased the survival rate, inhibited colony cells were further cultured for 20 min. After formation, arrested the cell cycle, and promot- the culture medium containing Hoechst33342 ed the apoptosis of SP cells. was removed, the plates were washed with the medium thrice and sorted using flow cy- Materials and methods tometry. Cell culture Cell cycle analysis Human MM Roswell Park Memorial Institute For the cell cycle analysis, each group of cells (RPMI)-8226 and NCI-H929 cell lines were was harvested, digested with trypsin, washed obtained from the American Type Culture Col- twice with PBS, and then centrifuged at 2000 lection (ATCC, Manassas, VA, USA) and cul- rpm for 5 min to collect the cells. Thereafter, tured in RPMI 1640 medium supplemented the cells were fixed with 70% precooled etha- with 10% (v/v) fetal bovine serum (FBS), 100 U/ nol at 4°C overnight, digested with 200 μg/ml ml penicillin, 100 µg/ml streptomycin, and 2 ribonuclease A at 37°C for 30 min, then 100 μl mmol/l L-glutamine (Gibco, Carlsbad, CA, USA). propidium iodide (PI) was added at 4°C in the All cells were maintained in a humidified incu- dark for 30 min. The samples were analyzed bator in a 5% CO2 atmosphere at 37°C. using flow cytometry (BD Biosciences, Franklin Lakes, NJ, USA) and the data were analyzed Cell viability assay using ModFit software. Cell viability was detected using a 3-(4,5-dimeth- Colony formation assay ylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay according to the manufacturer’s A colony formation assay was performed as protocol (Promega, Madison, WI, USA). Briefly, previously described [19]. Briefly, 2×104 RPMI- RPMI-8226 and NCI-H929 cells (5×103 cells/ 8226 and NCI-H929 cell suspensions were ml) were treated with various concentrations of resuspended in 0.8 ml growth medium con- DATS (Grade: reagent grade (RG); purity 98%; taining 0.3% low-melting-temperature agarose 5750 Int J Clin Exp Med 2017;10(3):5749-5756 DATS inhibits proliferation of side population cells in MM cells Figure 1. DATS reduced the survival rate of NCI-H929 and RPMI-8226 cells. (Promega, Madison, WI, USA) and treated with one-way analysis of variance (ANOVA) followed the drugs according to their grouping. The cells by a post-hoc LSD test. An independent t-test were then incubated in 24-well plates in tripli- was used to compare the differences between cate over a base layer of 0.8 ml growth medium groups. P-values <0.05 were considered statis- containing 0.6% low-melting-temperature aga- tically significant. rose. The plates were incubated for two weeks until colonies formed. The colonies were visual- Results ized and their number calculated using lightmi- croscopy (10×). The colony-forming efficiency DATS inhibited MM cell survival (CFE) percentage was calculated using the fol- lowing formula: The effect of DATS on the survival rate of MM cells was evaluated using an MTT assay. CFE = colony number ÷ inoculation cell number Treatment of RPMI-8226 and NCI-H929 cells ×100% for 1 to 3 days with 2, 5, 10, 20, 40, or 80 μM of DATS reduced the cell survival rate in a Apoptosis assay dose- and time-dependent manner (Figure 1). The IC values of DATS were 67.56, 44.77, and Apoptosis was detected using an apoptosis 50 detection kit (KeyGene, Nanjing, China). RPMI- 23.35 mg/L in NCI-H929 cells at 24, 48, and 72 h, respectively. The IC values of DATS were 8226 and NCI-H929 cells were collected after 50 centrifugation at 2000 rpm for 5 min.
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